Interpretive Summary: Important agricultural crops such as corn and wheat are pollinated by wind. Corn is monoecious, where both male and female flowers occur on a plant, and outcrosses, where pollen from one plant typically sire ovules on a different plant. In contrast, wheat has hermaphroditic flowers, where both male and female parts occur within a flower, and is a strong selfer, where pollen from one plant sires ovules on the same plant, typically the same flower on a plant. Both crops are tall, and are grown in open habitats, characteristics believed to favor the dispersal of pollen in wind-pollinated plants. Understanding the factors that select for wind pollination and unisexual flowers and whether one trait such as wind pollination tends to evolve before the other (unisexual flower) is important to breeders who, via artificial selection, modify plants to best serve humans’ needs. For example, could one ever contemplate developing a self-pollinated corn variety with hermaphroditic flowers or an outcross variety of wheat with monoecious flowers or insect-pollinated corn or wheat varieties? Understanding how these traits evolve and the selective forces responsible for trait transition represent a first step in answering such questions.

Technical Abstract:
Wind pollination is often associated with unisexual flowers, but which evolved first and played a causative role in the evolution of the other is unclear. The genus Thalictrum (Ranunculaceae) provides a unique system to examine the evolution of these traits because it contains both insect and wind pollination and a diversity of breeding systems. We used a phylogenetic approach to reconstruct ancestral states for breeding system, pollination mode, and geographic distribution in Thalictrum. We tested for correlated evolution to uncover which factors affected the evolution of unisexual flowers and wind pollination. We examined whether changes in one character preceded changes in another character or was affected by the state of the other character. Wind pollination evolved early and repeatedly within the genus, preceding the evolution of unisexual flowers in two cases. Dioecy evolved at least twice and has arisen directly from hermaphroditism. We observed no fully monoecious species in this group and andromonoecious and gynomoecious species in the genus represent terminal conditions that evolved directly from hermphroditism. Despite the strong correlations between wind pollination and unisexual flowers, wind pollination and New World distribution and unisexual flowers and New World distribution, our data could not tease apart whether, over the whole genus, wind pollination preceded the evolution of dioecy or unisexual flowers and whether wind pollination or dioecy originated prior to or after the dispersal to the New World. The lability of patterns of evolutionary transitions observed over the phylogeny put into question whether one particular sequence of evolutionary transition should be expected over single-genus or large-scale phylogenies or whether different evolutionary scenarios represent the rule rather than the exception.